Repeat proliferation and partial endoreplication jointly shape the patterns of genome size evolution in orchids

Abstract

Summary Although the evolutionary drivers of genome size change are known, the general patterns and mechanisms of plant genome size evolution are yet to be established. Here we aim to assess the relative importance of proliferation of repetitive DNA, chromosomal variation (including polyploidy), and the type of endoreplication for genome size evolution of the Pleurothallidinae, the most species‐rich orchid lineage. Phylogenetic relationships between 341 Pleurothallidinae representatives were refined using a target enrichment hybrid capture combined with high‐throughput sequencing approach. Genome size and the type of endoreplication were assessed using flow cytometry supplemented with karyological analysis and low‐coverage Illumina sequencing for repeatome analysis on a subset of samples. Data were analyzed using phylogeny‐based models. Genome size diversity (0.2–5.1 Gbp) was mostly independent of profound chromosome count variation (2n = 12–90) but tightly linked with the overall content of repetitive DNA elements. Species with partial endoreplication (PE) had significantly greater genome sizes, and genomic repeat content was tightly correlated with the size of the non‐endoreplicated part of the genome. In PE species, repetitive DNA is preferentially accumulated in the non‐endoreplicated parts of their genomes. Our results demonstrate that proliferation of repetitive DNA elements and PE together shape the patterns of genome size diversity in orchids.

Integrative Study of Genotypic and Phenotypic Diversity in the Eurasian Orchid Genus Neotinea

“…The size of the endoreplicated part of the genome appears to have broader evolutionary implications, as its uniformity among evolutionary lineages (Figure 3 and Table 1), except in recent polyploids, suggests some constraint on this trait, and the evolution of genome size is restricted to the non-endoreplicated part. This is consistent with the findings of Chumová et al (2021), who showed different rates of evolution for the endoreplicated and non-endoreplicated parts of genome in orchids from the subtribe Pleurothallidinae.…”

“…This study originally builds on our long-term research on orchids, specifically the causes and consequences of the unique trait of partial endoreplication (Trávníček et al, 2015(Trávníček et al, , 2019Hřibová et al, 2016;Chumová et al, 2021). By investigating the pattern of endoreplication in many orchid genera, we found that the smallest amount of the endoreplicated part of the genome in all orchids hitherto studied is observed in the N. lactea group (∼12-13%).…”

“…This phenomenon is known from all but one orchid subfamily (Trávníček et al, 2015) and is thought to be related to diversity in genome size and GC content (Trávníček et al, 2019). Only recently, it has been hypothesized that partial endoreplication is responsible for preferential replication of nonrepetitive DNA, possibly circumventing genome size constraints (Chumová et al, 2021). Partial endoreplication patterns have also been used to delimit taxa in some orchid genera (e.g., Trávníček et al, 2011), but their implications for other orchid groups have not been tested.…”

A chromosome-level, haplotype-phased Vanilla planifolia genome highlights the challenge of partial endoreplication for accurate whole-genome assembly

“…The fact that the gametes are haploid also suggests the presence of molecular mechanisms that enable the isolation of the holoploid genome. This type of endoreplication, which appears to be specific to the Orchidaceae lineage in plants, has been successively termed “progressively PE” ( Bory et al., 2008 ; Trávníček et al., 2015 ; Hřibová et al., 2016 ), strict PE ( Brown et al., 2017 ), and more recently, PE ( Chumová et al., 2021 ; Trávníček et al, 2019) . To be in line with the latest works and to harmonize the terminology for this phenomenon, the term PE will be used in this work.…”

“…It is very high in Vanilla pompona (F = 81%) but rather low in Vanilla mexicana (F = 17%) ( Brown et al., 2017 ). Several studies on orchids have also shown that species prone to PE have a larger genome than those prone to conventional endoreplication ( Trávníček et al., 2015 , 2019 ; Chumová et al., 2021 ). Nevertheless, the molecular mechanisms involved in PE are not yet elucidated.…”